Ethyl pyruvate-mediated Nrf2 activation and hemeoxygenase 1 induction in astrocytes confer protective effects via autocrine and paracrine mechanisms

Neurochemistry International

Volumn 61, Issue 1, 2012, Pages 89-99

  Shin, Joo Hyun ^a   Kim, Seung Woo ^a   Jin, Yinchuan ^a   Kim, Il Doo ^a   Lee, Ja Kyeong ^a  

^a Inha University School of Medicine   (South Korea)

Author keywords

Astrocytes; Ethyl pyruvate; GDNF; Hemeoxygenase 1; Nrf2

Indexed keywords

ANTIOXIDANT; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLUTATHIONE; HEMEOXYGENASE 1; OXYGENASE; PROTEIN KINASE B; PYRUVIC ACID DERIVATIVE; PYRUVIC ACID ETHYL ESTER; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; ASTROCYTE; AUTOCRINE EFFECT; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; ENZYME ACTIVITY; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ASTROCYTES; CELLS, CULTURED; CULTURE MEDIA; ENZYME INDUCTION; GLUTATHIONE; HEME OXYGENASE-1; HUMANS; MALE; NF-E2-RELATED FACTOR 2; PYRUVATES; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 84861469141     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2012.04.005     Document Type: Article

References (66)

1. P. Akerud, J.M. Canals, E.Y. Snyder, and E. Arenas Neuroprotection through delivery of glial cell line-derived neurotrophic factor by stem cells in a mouse model of Parkinson's disease J. Neurosci. 21 2001 8108 8118
2. J. Alam, and J.L. Cook Transcriptional regulation of the heme oxygenase-1 gene via the stress response element pathway Curr. Pharm. Des. 9 2003 2499 2511
3. R. Beschorner, D. Adjodah, J.M. Schwab, M. Mittelbronn, I. Pedal, R. Mattern, H.J. Schluesener, and R. Meyermann Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain in humans Acta Neuropathol. 100 2000 377 384
4. V. Calabrese, A. Ravagna, C. Colombrita, G. Scapagnini, E. Guaqliano, M. Calvani, D.A. Butterfield, and A.M. Giuffrida Stella Acetylcarnitine induces heme oxygenase in rat astrocytes and protects against oxidative stress: involvement of the transcription factor Nrf2 J. Neurosci. Res. 79 2005 509 521
5. M.J. Calkins, D.A. Johnson, J.A. Townsend, M.R. Vargas, J.A. Dowell, T.P. Williamson, A.D. Kraft, J.M. Lee, J. Li, and J.A. Johnson The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease Antioxid. Redox Signaling 11 2009 497 508
6. M.J. Calkins, M.R. Vargas, D.A. Johnson, and J.A. Johnson Astrocyte-specific overexpression of Nrf2 protects striatal neurons from mitochondrial complex II inhibition Toxicol. Sci. 115 2010 557 568
7. E.E. Capowski, B.L. Schneider, A.D. Ebert, C.R. Seehus, J. Szulc, R. Zufferey, P. Aebischer, and C.N. Svendsen Lentiviral vector-mediated genetic modification of human neural progenitor cells for ex vivo gene therapy J. Neurosci. Methods 163 2007 338 349
8. K. Chen, K. Gunter, and M.D. Maines Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death J. Neurochem. 75 2000 304 313
9. P.C. Chen, M.R. Vargas, A.K. Pani, R.J. Smeyne, D.A. Johnson, Y.W. Kan, and J.A. Johnson Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: critical role for the astrocyte Proc. Natl. Acad. Sci. USA 106 2009 2933 2938
10. J. Chen-Roetling, L. Benvenisti-Zarom, and R.F. Regan Cultured astrocytes from heme oxygenase-1 knockout mice are more vulnerable to heme-mediated oxidative injury J. Neurosci. Res. 82 2005 802 810
11. I.H. Cho, S.W. Kim, J.B. Kim, T.K. Kim, K.W. Lee, P.L. Han, and J.K. Lee Ethyl pyruvate attenuates kainic acid-induced neuronal cell death in the mouse hippocampus J. Neurosci. Res. 84 2006 1505 1511
12. C.M. Clements, R.S. Mcnally, B.J. Conti, T.W. Mak, and J.P. Ting DJ-1, a cancer- and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2 Proc. Natl. Acad. Sci. USA 103 2006 15091 15096
13. A. Cuadrado, and A.I. Rojo Heme oxygenase-1 as a therapeutic target in neurodegenerative diseases and brain infections Curr. Pharm. Des. 14 2008 429 442
14. L.A. Cunningham, and C. Su Astrocyte delivery of glial cell line-derived neurotrophic factor in a mouse model of Parkinson's disease Exp. Neurol. 174 2002 230 242
15. S.H. Davé, J.S. Tilstra, K. Matsuoka, F. Li, R.A. DeMarco, D. Beer-Stolz, A.R. Sepulveda, M.P. Fink, M.T. Lotze, and S.E. Plevy Ethyl pyruvate decreases HMGB1 release and ameliorates murine colitis J. Leukoc. Biol. 86 2009 633 643
16. R. Di Paola, E. Mazzon, M. Galuppo, E. Esposito, P. Bramanti, M.P. Fink, and S. Cuzzocrea Ethyl pyruvate therapy attenuates experimental severe arthritis caused by type II collagen (CII) in the mouse (CIA) Int. J. Immunopathol. Pharmacol. 23 2010 1087 1098
17. Z. Dong, Y. Lavrovsky, M.A. Venkatachalam, and A.K. Roy Heme oxygenase-1 in tissue pathology: the Yin and Yang Am. J. Pathol. 156 2000 1485 1488
18. R. Dringen, J.M. Gutterer, and J. Hirrlinger Glutathione metabolism in brain metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species Eur. J. Biochem. 267 2000 4912 4916
19. A.L. Eggler, G. Liu, J.M. Pezzuto, R.B. van Breemen, and A.D. Mesecar Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2 Proc. Natl. Acad. Sci. USA 102 2005 10070 10075
20. M.P. Fink Ethyl pyruvate: a novel anti-inflammatory agent J. Intern. Med. 261 2007 349 362
21. L. Gan, D.A. Johnson, and J.A. Johnson Keap-1-Nrf2 activation in the presence and absence of DJ-1 Eur. J. Neurosci. 31 2010 967 977
22. P.J. Gebicke-Haerter, J. Bauer, A. Schobert, and H. Northoff Lipopolysaccharide-free conditions in primary astrocyte cultures allow growth and isolation of microglial cells J. Neurosci. 9 1989 183 194
23. O.W. Griffith Biologic and pharmacologic regulation of mammalian glutathione synthesis Free Radic. Biol. Med. 27 1999 922 935
24. Y. Han, J.A. Englert, R. Yang, R.L. Delude, and M.P. Fink Ethyl pyruvate inhibits nuclear factor-kappaB-dependent signaling by directly targeting p65 J. Pharmacol. Exp. Ther. 312 2005 1097 1105
25. S.A. Harvey, E. Guerriero, N. Charukamnoetkanok, J. Piluek, J.S. Schuman, and N. Sundarraj Response of cultured human keratocytes and myofibroblasts to ethyl pyruvate: a microarray analysis of gene expression Invest. Opthalmol. Vis. Sci. 51 2010 2917 2927
26. J.D. Hayes, and M. McMahon NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer Trends Biochem. Sci. 34 2009 176 188
27. S.Y. Hung, H.C. Liou, K.H. Kang, R.M. Wu, C.C. Wen, and W.M. Fu Overexpression of heme oxygenase-1 protects dopaminergic neurons against 1-methyl-4-phenylpyridinium-induced neurotoxicity Mol. Pharmacol. 74 2008 1564 1575
28. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, and M. Yamamoto Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Nef2 domain Genes Dev. 13 1999 76 86
29. A.K. Jaiswal Regulation of gene encoding NAD(P)H:quinone oxidoreductases Free Radic. Biol. Med. 29 2000 254 262
30. Jang, H.J., Kim, Y.M., Tsoyi, K., Park, E.J., Lee, Y.S., Kim, H.J., Lee, J.H., Joe, Y., Chung, H.T., Chang, K.C., 2012. Ethyl pyruvate induces HO-1 through p38 MAPK activation by depletion of glutathione in RAW 264.7 cells and improves survival in septic animals. Antioxid. Redox. Signal. [Epub ahead of print].
31. J. Jeyapaul, and A.K. Jaiswal Nrf2 and c-Jun regulation of antioxidant response element (ARE)-mediated expression and induction of gamma- glutamylcysteine synthetase heavy subunit gene Biochem. Pharmacol. 59 2000 1433 1439
32. A.S. Johansson, K. Johansson-Haque, S. Okret, and J. Palmblad Ethyl pyruvate modulates acute inflammatory reactions in human endothelial cells in relation to the NF-kB pathway Br. J. Pharmacol. 154 2008 1318 1326
33. K. Kanninen, R. Heikkinen, T. Malm, T. Rolova, S. Kuhmonen, H. Leinonen, S. Ylä-Herttuala, H. Tanila, A.L. Levonen, M. Koistinaho, and J. Koistinaho Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse of Alzheimer's disease Proc. Natl. Acad. Sci. USA 106 2009 16505 16510
34. J.W. Kaspar, S.K. Niture, and A.K. Jaiswal Nrf2:INrf2 (Keap1) signaling in oxidative stress Free Radic. Biol. Med. 47 2009 1304 1309
35. H.S. Kim, I.H. Cho, J.E. Kim, Y.J. Shin, J.H. Jeon, Y. Kim, Y.M. Yang, K.H. Lee, J.W. Lee, W.J. Lee, S.K. Ye, and M.H. Chung Ethyl pyruvate has an anti-inflammatory effect by inhibiting ROS-dependent STAT signaling in activated microglia Free Radic. Biol. Med. 45 2008 950 963
36. S.W. Kim, J.Y. Jeong, H.J. Kim, J.S. Seo, P.L. Han, S.H. Yoon, and J.K. Lee Combination treatment with ethyl pyruvate and aspirin enhances neuroprotection in the postischemic brain Neurotox. Res. 17 2010 39 49
37. C.W. Kung, Y.M. Lee, P.Y. Cheng, Y.J. Peng, and M.H. Yen Ethyl pyruvate reduces acute lung injury via regulation of iNOS and HO-1 expression in endotoxemic rats J. Surg. Res. 167 2011 e323 e331
38. W.D. Le, W.J. Xie, and S.H. Appel Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury J. Neurosci. Res. 56 1999 652 658
39. E.J. Lee, and H.S. Kim Inhibitory mechanism of MMP-9 gene expression by ethyl pyruvate in lipopolysaccharide-stimulated BV2 microglial cells Neurosci. Lett. 493 2011 38 43
40. P.J. Lee, J. Alam, G.W. Wiegand, and A.M. Choi Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia Proc. Natl. Acad. Sci. USA 93 1996 10393 10398
41. W. Li, S.W. Yu, and A.N. Kong Nrf2 possesses a redox-sensitive nuclear exporting signal in the Neh5 transactivation domain J. Biol. Chem. 15 2006 27251 27263
42. Y. Lin, H.J. Vreman, R.J. Wong, T. Tjoa, T. Yamauchi, and L.J. Noble-Haeusslein Heme oxygenase-1 stabilizes the blood-spinal cord barrier and limits oxidative stress and white matter damage in the acutely injured murine spinal cord J. Cereb. Blood Flow Metab. 27 2007 1010 1021
43. Y. Liu, B. Zhu, X. Wan, L. Lou, P. Li, D.W. Paty, and M.S. Cynader Bilirubin as a potent antioxidant suppresses experimental autoimmune encephalomyelitis: implications for the role of oxidative stress in the development of multiple sclerosis J. Neuroimmunol. 139 2003 27 35
44. J. Liu, M. Segal, S. Yoo, G.Y. Yang, M. Kelly, T.L. James, and L. Litt Antioxidant effect of ethyl pyruvate in respiring neonatal cerebrocortical slices after H(2)O(2) stress Neurochem. Int. 54 2009 106 110
45. M.D. Maines Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications FASEB J. 2 1988 2557 2568
46. M.D. Maines, B. Polevoda, T. Coban, K. Johnson, S. Stoliar, T.J. Huang, N. Panahian, D.A. Cory-Slechta, and W.K. McCoubrey Jr. Neuronal overexpression of heme oxygenase-1 correlates with an attenuated exploratory behavior and causes an increase in neuronal NADPH diaphorase staining J. Neurochem. 70 1998 2057 2069
47. D. Martin, A.I. Rojo, M. Salinas, R. Diaz, G. Gallardo, J. Alam, C.M. De Galarreta, and A. Cuadrado Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the nrf2 transciption factor in response to the antioxidant phytochemical carnosol J. Biol. Chem. 279 2004 8919 8929
48. H. Motohashi, and M. Yamamoto Nrf2-Keap1 defines a physiologically important stress response mechanism Trends Mol. Med. 10 2004 549 557
49. T. Nguyen, P.J. Sherratt, and C.B. Pickett Regulatory mechanisms controlling gene expression mediated by the antioxidant response element Annu. Rev. Pharmacol. Toxicol. 43 2003 233 260
50. T. Nguyen, P. Nioi, and C.B. Pickett The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress J. Biol. Chem. 284 2009 13291 13295
51. N. Panahian, M. Yoshiura, and M.D. Maines Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice J. Neurochem. 72 1999 1187 1203
52. C.P. Ramsey, C.A. Glass, M.B. Montgomery, K.A. Lindl, G.P. Ritson, L.A. Chia, R.L. Hamilton, C.T. Chu, and K.L. Jordan-Sciutto Expression of Nrf2 in neurodegenerative disease J. Neuropathol. Exp. Neurol. 66 2007 75 85
53. S.W. Ryter, and A.M. Choi Heme oxygenase-1: molecular mechanisms of gene expression in oxygen-related stress Antioxid. Redox Signaling 4 2002 625 632
54. J.K. Sandhu, M. Gardaneh, R. Iwasiow, P. Lanthier, S. Gangaraju, M. Ribecco-Lutkiewicz, R. Tremblay, K. Kiuchi, and M. Sikorska Astrocyte-secreted GDNF and glutathione antioxidant system protect neurons against 6OHDA cytotoxicity Neurobiol. Dis. 33 2009 405 414
55. H.M. Schipper, A. Gupt, and W.A. Szarek Suppression of glial HO-1 activity as a potential neurotherapeutic intervention in AD Curr. Alzheimer Res. 6 2009 424 430
56. A.Y. Shih, D.A. Johnson, G. Wong, A.D. Kraft, L. Jiang, H. Erb, J.A. Johnson, and T.H. Murphy Coordinate regulation of glutathione biosynthesis and release by Nrf2-exporessing glia potently protects neurons from oxidative stress J. Neurosci. 23 2003 3394 3406
57. M. Song, J.A. Kellum, H. Kaldas, and M.P. Fink Evidence that glutathione depletion is a mechanism responsible for the anti-inflammatory effects of ethyl pyruvate in cultured lipopolysaccharide-stimulated RAW 264.7 cells J. Pharmacol. Exp. Ther. 308 2004 307 316
58. A. Takeda, G. Perry, N.G. Abraham, B.E. Dwyer, R.K. Kutty, J.T. Laitinen, R.B. Petersen, and M.A. Smith Overexpression of heme oxygenase in neuronal cells, the possible interaction with Tau J. Biol. Chem. 275 2000 5395 5399
59. NTR-dependent motor neuron apoptosis J. Neurochem. 97 2006 687 696
60. H.Q. Wang, Y.Z. Xu, and C.Q. Zhu Upregulation of heme oxygenase-1 by acteoside through ERK and PI3 K/Akt pathway confer neuroprotection against beta-amyloid-induced neurotoxicity Neurotox. Res. 21 2012 368 378
61. A.C. Wild, H.R. Moinova, and R.T. Mulcahy Regulation of γ-glutamylcysteine synthetase regulatory subunit gene expression by the transcription factor J. Biol. Chem. 274 1999 33627 33636
62. D. Willis, A.R. Moore, R. Frederick, and D.A. Willoughby Heme oxygenase: a novel target for the modulation of the inflammatory response Nat. Med. 2 1996 87 90
63. J.X. Wilson Antioxidant defense of the brain: a role for astrocytes Can. J. Physiol. Pharmacol. 75 1997 1149 1163
64. Y.M. Yu, J.B. Kim, K.W. Lee, S.Y. Kim, P.L. Han, and J.K. Lee Inhibition of the cerebral ischemic injury by ethyl pyruvate with a wide therapeutic window Stroke 26 2005 2238 2243
65. D.D. Zhang Mechanistic studies of Nrf2-Keap1 signaling pathway Drug Metab. Rev. 38 2006 769 789
66. D.D. Zhang, and M. Hannink Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress Mol. Cell Biol. 23 2003 8137 8151